Specific contribution of the erythropoietin gene 3' enhancer to hepatic erythropoiesis after late embryonic stages
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Erythropoietin (Epo) is secreted from the liver and kidney, where Epo production is strictly regulated at the transcriptional level in a hypoxia- and/or anemia-inducible manner. Here, we examined the in vivo function of the enhancer located 3' to the Epo gene (EpoE-3'). Reporter transgenic-mouse analyses revealed that the EpoE-3' enhancer is necessary and sufficient for the liver-specific and hypoxia-responsive expression of the gene after embryonic day 14.5 (E14.5). However, the enhancer is dispensable for Epo gene expression in the kidney and early-stage embryonic liver. Genetic removal of EpoE-3' from the endogenous Epo gene resulted in mice with severe anemia at late embryonic and neonatal stages due to defects in hepatic erythropoiesis, but early hepatic and splenic erythropoiesis was not affected. The mutant mice recover from the anemia in the juvenile period when major Epo production switches from the liver to the kidney. These results demonstrate that EpoE-3' is necessary for late hepatic erythropoiesis by specifically supporting paracrine production of Epo in the liver. In contrast, Epo production in the kidney utilizes distinct regulatory machinery and supports erythropoiesis in the bone marrow and spleen in adult animals.
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The 3′-hypoxia enhancer region is absolutely required for hypoxic induction of Epo in the liver in mice.
“The 3′-hypoxia enhancer region is absolutely required for the hypoxic induction of Epo in the liver, as shown by genetic studies in mice. 18”
From Regulation of erythropoiesis by hypoxia-inducible factors (2013) · cites this paper as [18]
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Diverse of Erythropoiesis Responding to Hypoxia and Low Environmental Temperature in Vertebrates
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Efficacy estimation of erythropoiesis-stimulating agents using erythropoietin-deficient anemic mice
Suzuki, N., Sasaki, Y., Kato, K., Yamazaki, S., Kurasawa, M., Yorozu, K., Shimonaka, Y., & Yamamoto, M. P. (2016) · Haematologica · doi:10.3324/haematol.2015.140814 · Cited by 16 · see citing works
Nakai, T., Saigusa, D., Kato, K., Fukuuchi, T., Koshiba, S., Yamamoto, M. P., & Suzuki, N. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122641 · Cited by 13 · see citing works
Spatiotemporal dynamics of fetal liver hematopoietic niches
Peixoto, M. M., Soares‐da‐Silva, F., Bonnet, V., Zhou, Y., Ronteix, G., Santos, R. F., Mailhé, M.-P., Nogueira, G., Feng, X., Pereira, J. P., et al. (2024) · The Journal of Experimental Medicine · doi:10.1084/jem.20240592 · Cited by 12 · see citing works
Identification of Hepatic-like EPO as a Cause of Polycythemia
Martin, L., Maric, D., Idriss, S., Delamare, M., Roy, A. L., Maaziz, N., Caillaud, A., Si‐Tayeb, K., Robriquet, F., Lenglet, M., et al. (2025) · New England Journal of Medicine · doi:10.1056/nejmoa2414954 · Cited by 13 · see citing works
Suzuki, N., Mukai, H. Y., & Yamamoto, M. P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119442 · Cited by 13 · see citing works
ARID1A loss in adult hepatocytes activates β-catenin-mediated erythropoietin transcription
Riou, R., Ladli, M., Gerbal-Chaloin, S., Bossard, P., Gougelet, A., Godard, C., Loesch, R., Lagoutte, I., Lager, F., Calderaro, J., et al. (2020) · eLife · doi:10.7554/elife.53550 · Cited by 12 · see citing works
Kai, S., Tanaka, T., Matsuyama, T., Suzuki, K., & Hirota, K. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.03.020 · Cited by 12 · see citing works
Motojima, M., Tanaka, M., & Kume, T. (2022) · Journal of Cell Science · doi:10.1242/jcs.260356 · Cited by 9 · see citing works
Yamazaki, S., Hirano, I., Kato, K., Yamamoto, M. P., & Suzuki, N. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119075 · Cited by 8 · see citing works
Crosstalk between oxygen signaling and iron metabolism in renal interstitial fibroblasts
Suzuki, N., Iwamura, Y., Kato, K., Ishioka, H., Konta, Y., Sato, K., Uchida, N., Koida, N., Sekine, H., Tanaka, T., et al. (2024) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.24-8 · Cited by 8 · see citing works
Iwamura, Y., Nakai, T., Kato, K., Ishioka, H., Yamamoto, M. P., Hirano, I., & Suzuki, N. (2024) · Molecular and Cellular Biology · doi:10.1080/10985549.2024.2428717 · Cited by 8 · see citing works
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Defective Slc7a7 transport reduces erythropoietin compromising erythropoiesis and iron homeostasisPreprint
Giroud‐Gerbetant, J., Sotillo, F., Hernández, G., Lynch, C. J., Ruano, I., Siri, B., Sebastián, D., Zorzano, A., Artuch, R., Ormazábal, A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.15.456393 · Cited by 2 · see citing works
Single-nucleotide polymorphisms in EPO 5′ hypoxia response elements associated with anemia
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Iwamura, Y., Nakai, T., Kato, K., Ishioka, H., Yamamoto, M. P., Hirano, I., & Suzuki, N. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.02.28.582479 · Cited by 1 · see citing works
Updates in the management of diabetic nephropathy
Prakash, J. (2015) · Clinical Queries Nephrology · doi:10.1016/j.cqn.2015.11.001
Perrin‐Terrin, A. (2018) · doi:10.70675/e19e922bz4ab1z4df2z8e00z839db7c46630
- Authors
- Suzuki, N., Obara, N., Pan, X., Watanabe, M., Jishage, K.-I., Minegishi, N., & Yamamoto, M.
- Affiliations
- University of Tsukuba (JP)
- Chugai Pharmaceutical Co., Ltd. (Japan) (JP)
- Tohoku University (JP)
- Corresponding author
- Yamamoto, Masayuki
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 2011-09
- Volume
- 31
- Issue
- 18
- Pages
- 3896-3905
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC3165733
- OpenAlex
- W2119394080
- Cited by
- 65
- References
- 54
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 7 · 2023: 1 · 2022: 2 · 2021: 5 · 2020: 3 · 2019: 4 · 2018: 6 · 2017: 2 · 2016: 5 · 2015: 13 · 2014: 3 · 2013: 9
- FWCI
- 2.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- University of Tsukuba
- Japan Society for the Promotion of Science (19GS0312, 21591216, 22790895)
- Exploratory Research for Advanced Technology
- Topics
- Health Sciences › Medicine › Hematology › Erythropoietin and Anemia Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
- Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
- Keywords
- erythropoietin, liver-specific gene expression, transcriptional regulation
- MeSH terms
- Anemia, Animals, Enhancer Elements, Genetic, Erythropoiesis, Erythropoietin, Kidney, Liver, Mice, Transgenic, Regulatory Sequences, Nucleic Acid, Gene Expression, Polymerase Chain Reaction, Gene Expression Regulation, Developmental, Hepatocytes, 3' Flanking Region, Chromatin Immunoprecipitation, Mice, Gene Knockout Techniques
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